Immunotherapy for urothelial cancer: from the diagnostic pathologist’s point of view

References

• Mehta K, Patel K, Parikh RA. Immunotherapy in genitourinary malignancies. J Hematol Oncol. 2017;10(1):95.
   PubMedGoogle Scholar
• Gevaert T, Montironi R, Lopez-Beltran A, et al. Genito-urinary genomics and emerging biomarkers for immunomodulatory cancer treatment. Semin Cancer Biol. 2018;52(Pt 2):216–227.
   PubMedGoogle Scholar
• Three drugs approved for urothelial carcinoma by FDA | cancer discovery. [cited 2018 Apr 18]. Available from: http://cancerdiscovery.aacrjournals.org/content/7/7/659
   Google Scholar
• Bilgin B, Sendur MA, Hizal M, et al. An update on immunotherapy options for urothelial cancer. Expert Opin Biol Ther. 2019;19:1265–1274.
   PubMed Web of Science ®Google Scholar
• Zlotta AR, Fleshner NE, Jewett MA. The management of BCG failure in non-muscle-invasive bladder cancer: an update. Can Urol Assoc J. 2009;3(6 Suppl 4):S199–205.
   PubMedGoogle Scholar
• Balar AV, Kulkarni GS, Uchio EM, et al. Keynote 057: phase II trial of Pembrolizumab (pembro) for patients (pts) with high-risk (HR) nonmuscle invasive bladder cancer (NMIBC)unresponsive to bacillus calmette-guérin (BCG). J Clin Oncol. 2019;37(7_suppl): 350–350. DOI:10.1200/JCO.2019.37.7_suppl.350
   PubMed Web of Science ®Google Scholar
• FDA limits the use of Tecentriq and Keytruda for some urothelial cancer patients. Available from: https://www.fda.gov/drugs/informationondrugs/approveddrugs/ucm612484.htm
   Google Scholar
• Gevaert T, Eckstein M, Montironi R, et al. Re: Maud Rijnders, Astrid A.M. van der Veldt, Tahlita C.M. Zuiverloon, et al. PD-L1 antibody comparison in urothelial carcinoma. Eur Urol. in press. https://doi.10.1016/j.eururo.2018.11.002. Eur Urol. 2019. DOI:10.1016/j.eururo.2019.01.038
   PubMedGoogle Scholar
• Hirsch FR, McElhinny A, Stanforth D, et al. PD-L1 immunohistochemistry assays for lung cancer: results from phase 1 of the blueprint PD-L1 IHC assay comparison project. J Thorac Oncol. 2017;12(2):208–222.
   PubMed Web of Science ®Google Scholar
• Tsao MS, Kerr KM, Kockx M, et al. PD-L1 Immunohistochemistry comparability study in real-life clinical samples: results of blueprint phase 2 project. J Thorac Oncol. 2018;13(9):1302–1311.
   PubMed Web of Science ®Google Scholar
• Adam J, Le Stang N, Rouquette I, et al. Multicenter harmonization study for PD-L1 IHC testing in non-small-cell lung cancer. Ann Oncol. 2018;29(4):953–958.
   PubMed Web of Science ®Google Scholar
• Tretiakova M, Fulton R, Kocherginsky M, et al. Concordance study of PD-L1 expression in primary and metastatic bladder carcinomas: comparison of four commonly used antibodies and RNA expression. Mod Pathol. 2018;31(4):623–632.
   PubMed Web of Science ®Google Scholar
• Zavalishina L, Tsimafeyeu I, Povilaitite P, et al. RUSSCO-RSP comparative study of immunohistochemistry diagnostic assays for PD-L1 expression in urothelial bladder cancer. Virchows Arch. 2018;473(6):719–724.
   PubMed Web of Science ®Google Scholar
• Zajac M, Scott M, Ratcliffe M, et al. Concordance among four commercially available, validated programmed cell death ligand-1 assays in urothelial carcinoma. Diagn Pathol. 2019;14(1):99.
   PubMed Web of Science ®Google Scholar
• Hodgson A, Slodkowska E, Jungbluth A, et al. PD-L1 immunohistochemistry assay concordance in urothelial carcinoma of the bladder and hypopharyngeal squamous cell carcinoma. Am J Surg Pathol. 2018;42(8):1059–1066.
   PubMed Web of Science ®Google Scholar
• Rijnders M, van der Veldt AAM, Zuiverloon TCM, et al. PD-L1 antibody comparison in urothelial carcinoma. Eur Urol. 2019;75(3):538–540.
   PubMed Web of Science ®Google Scholar
• Eckstein M, Erben P, Kriegmair MC, et al. Performance of the Food and Drug Administration/EMA-approved programmed cell death ligand-1 assays in urothelial carcinoma with emphasis on therapy stratification for first-line use of atezolizumab and pembrolizumab. Eur J Cancer. 2019;106:234–243.
   PubMed Web of Science ®Google Scholar
• Aggen DH, Drake CG. Biomarkers for immunotherapy in bladder cancer: a moving target. J Immunother Cancer. 2017;5(1):94.
   PubMedGoogle Scholar
• Wang Y, Wang H, Yao H, et al. Regulation of PD-L1: emerging routes for targeting tumor immune evasion. Front Pharmacol. 2018;9:536.
   PubMed Web of Science ®Google Scholar
• Moch H, Humphrey PA, Ulbright TM, et al. WHO classification of tumours of the urinary system and male genital organs. 4th ed. Lyon: IARC; 2016.
   Google Scholar
• Lopez-Beltran A, Cheng L, Raspollini MR, et al. Variants of bladder cancer: the pathologist’s point of view. Eur Urol Suppl. 2017;16:210–222.
   Web of Science ®Google Scholar
• Amin MB. Histological variants of urothelial carcinoma: diagnostic, therapeutic and prognostic implications. Mod Pathol. 2009;22(Suppl 2):S96–S118.
   PubMedGoogle Scholar
• Lopez-Beltran A, Henriques V, Montironi R, et al. Variants and new entities of bladder cancer. Histopathology. 2019;74:77–96.
   PubMed Web of Science ®Google Scholar
• Udager AM, McDaniel AS, Hovelson DH, et al. Frequent PD-L1 protein expression and molecular correlates in urinary bladder squamous cell carcinoma. Eur Urol. 2018;74(4):529–531.
   PubMed Web of Science ®Google Scholar
• Reis H, Serrette R, Posada J, et al. PD-L1 expression in urothelial carcinoma with predominant or pure variant histology: concordance among 3 commonly used and commercially available antibodies. Am J Surg Pathol. 2019;43(7):920–927.
   PubMed Web of Science ®Google Scholar
• Necchi A, Anichini A, Raggi D, et al. Pembrolizumab as neoadjuvant therapy before radical cystectomy in patients with muscle-invasive urothelial bladder carcinoma (PURE-01): an open-label, single-arm, phase II study. J Clin Oncol. 2018;36(34):3353–3360.
   Google Scholar
• Necchi A, Raggi D, Gallina A, et al. Updated results of PURE-01 with preliminary activity of neoadjuvant pembrolizumab in patients with muscle-invasive bladder carcinoma with variant histologies. Eur Urol. 2019. pii: S0302-2838(19)30825-5.
   Web of Science ®Google Scholar
• Li H, Zhang Q, Shuman L, et al. Evaluation of PD-L1 and other immune markers in bladder urothelial carcinoma stratified by histologic variants and molecular subtypes. Sci Rep. 2020;10(1439). DOI:10.1038/s41598-020-58351-6
   Google Scholar
• Joseph RW, Millis SZ, Carballido EM, et al. PD-1 and PD-L1 expression in renal cell carcinoma with sarcomatoid differentiation. Cancer Immunol Res. 2015;3(12):1303–1307.
   PubMed Web of Science ®Google Scholar
• Velcheti V, Rimm DL, Schalper KA. Sarcomatoid lung carcinomas show high levels of programmed death ligand-1 (PD-L1). J Thorac Oncol. 2013;8(6):803–805.
   PubMed Web of Science ®Google Scholar
• Necchi A, Madison R, Raggi D, et al. Comprehensive assessment of immuno-oncology biomarkers in adenocarcinoma, urothelial carcinoma, and squamous-cell carcinoma of the bladder. Eur Urol. 2020. pii: S0302-2838(20)30003-8.
   Web of Science ®Google Scholar
• Sjödahl G, Jackson CL, Bartlett JM, et al. Molecular profiling in muscle-invasive bladder cancer: more than the sum of its parts. J Pathol. 2019;247(5):563–573.
   PubMed Web of Science ®Google Scholar
• Cancer Genome Atlas Research Network. Comprehensive molecular characterization of urothelial bladder carcinoma. Nature. 2014;507(7492):315–322.
   PubMed Web of Science ®Google Scholar
• Dadhania V, Zhang M, Zhang L, et al. Meta-analysis of the luminal and basal subtypes of bladder cancer and the identification of signature immunohistochemical markers for clinical use. EBioMedicine. 2016;12:105–117.
   PubMed Web of Science ®Google Scholar
• Breyer J, Wirtz RM, Otto W, et al. In stage pT1 nonmuscle- invasive bladder cancer (NMIBC), high KRT20 and low KRT5 mRNA expression identify the luminal subtype and predict recurrence and survival. Virchows Arch. 2017;470:267–274.
   PubMed Web of Science ®Google Scholar
• Balar AV, Galsky MD, Rosenberg JE, et al. Atezolizumab as first-line treatment in cisplatin-ineligible patients with locally advanced and metastatic urothelial carcinoma: a single-arm, multicentre, phase 2 trial. Lancet. 2017;389(10064):67–76.
   PubMed Web of Science ®Google Scholar
• Hodgson A, Liu SK, Vesprini D, et al. Basal-subtype bladder tumours show a ‘hot’ immunophenotype. Histopathology. 2018;73(5):748–757.
   PubMed Web of Science ®Google Scholar
• Pfannstiel C, Strissel PL, Chiappinelli KB, et al. The tumor immune microenvironment drives a prognostic relevance that correlates with bladder cancer subtypes. Cancer Immunol Res. 2019;7(6):923–938.
   PubMed Web of Science ®Google Scholar
• Tan TZ, Rouanne M, Tan KT, et al. Molecular subtypes of urothelial bladder cancer: results from a meta-cohort analysis of 2411 tumors. Eur Urol. 2019;75(3):423–432.
   PubMed Web of Science ®Google Scholar
• Mariathasan S, Turley SJ, Nickles D, et al. TGF-β attenuates tumour response to PD-L1 blockade by contributing to exclusion of T cells. Nature. 2018;554:544–548.
   PubMed Web of Science ®Google Scholar
• Miyamoto DT, Gibb E, Mouw KW, et al. Genomic profiling of muscle invasive bladder cancer to predict response to bladder-sparing trimodality therapy. Genitourinary Cancers Symposium. San Francisco: ASCO; 2018. DOI:10.1200/JCO.2018.36.6_suppl.513
   Google Scholar
• Sweis RF, Spranger S, Bao R, et al. Molecular drivers of the non-T-cell-inflamed tumor microenvironment in Urothelial bladder cancer. Cancer Immunol Res. 2016;4:563–568.
   PubMed Web of Science ®Google Scholar
• Gajewski TF. The next hurdle in cancer immunotherapy: overcoming the non-T-cell-inflamed tumor microenvironment. Semin Oncol. 2015;42:663–671.
   PubMed Web of Science ®Google Scholar
• Ayers M, Lunceford J, Nebozhyn M, et al. IFN-gamma-related mRNA profile predicts clinical response to PD-1 blockade. J Clin Invest. 2017;127(8):2930–2940.
   PubMed Web of Science ®Google Scholar
• Diaz LA, Marabelle A, Delord J-P, et al. Pembrolizumab therapy for microsatellite instability high (MSI-H) colorectal cancer (CRC) and non-CRC. J Clin Oncol. 2017;35:3071.
   Web of Science ®Google Scholar
• Shah MA, Bennouna J, Shen L, et al. Pembrolizumab for previously treated metastatic adenocarcinoma or squamous cell carcinoma of the esophagus: phase 2 KEYNOTE-180 study. J Clin Oncol. 2016;34:TPS4139–TPS.
   Google Scholar
• Doi T, Bennouna J, Shen L, et al. KEYNOTE-181: phase 3, open-label study of second-line pembrolizumab vs single-agent chemotherapy in patients with advanced/metastatic esophageal adenocarcinoma. J Clin Oncol. 2016;34:TPS4140–TPS.
   Google Scholar
• Schalper KA, Kaftan E, Herbst RS. Predictive biomarkers for PD-1 axis therapies: the hidden treasure or a call for research. Clin Cancer Res. 2016;22:2102–2104.
   PubMed Web of Science ®Google Scholar
• Lovitch SB, Rodig SJ. The role of surgical pathology in guiding cancer immunotherapy. Annu Rev Pathol. 2016;11:313–341.
   PubMed Web of Science ®Google Scholar